Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites

Nature Communications

Volumn 6, Issue , 2015, Pages

  Thorburn, Alison N ^a   McKenzie, Craig I ^a   Shen, Sj ^a   Stanley, Dragana ^b   MacIa, Laurence ^a   Mason, Linda J ^a   Roberts, Laura K ^a   Wong, Connie H Y ^a   Shim, Raymond ^a   Robert, Remy ^a   Chevalier, Nina ^a,c   Tan, Jian K ^a   Marinõ, Eliana ^a   Moore, Rob J ^a,d   Wong, Lee ^a   McConville, Malcolm J ^e   Tull, Dedreia L ^e   Wood, Lisa G ^f   Murphy, Vanessa E ^f   Mattes, Joerg ^f   Gibson, Peter G ^f   MacKay, Charles R ^a,g   more..

^a MONASH UNIVERSITY   (Australia)

^b CENTRAL QUEENSLAND UNIVERSITY   (Australia)

^c UNIVERSITY OF FREIBURG   (Germany)

^d CSIRO   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

^f UNIVERSITY OF NEWCASTLE   (Australia)

^g UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; HISTONE DEACETYLASE 9; ACETIC ACID DERIVATIVE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; HDAC9 PROTEIN, MOUSE; HISTONE DEACETYLASE; REPRESSOR PROTEIN; VOLATILE FATTY ACID;

ARTIFICIAL DIET; ASTHMA; DISEASE CONTROL; DISEASE INCIDENCE; GENE EXPRESSION; GERM CELL; HERITABILITY; MATERNAL HEALTH; METABOLITE; MICROBIAL COMMUNITY; PREGNANCY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; CONTROLLED STUDY; EPIGENETICS; FEMALE; GENE EXPRESSION; HIGH FIBER DIET; INTESTINE FLORA; MALE; MATERNAL NUTRITION; METABOLITE; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; ACETYLATION; ANIMAL; CYTOLOGY; DIET; DIETARY FIBER; DISEASE MODEL; DRUG EFFECTS; GENETIC EPIGENESIS; GENETICS; IMMUNOLOGY; METABOLISM; PREGNANCY; PRENATAL EXPOSURE; PROMOTER REGION;

BACTERIA (MICROORGANISMS); MUS;

ACETATES; ACETYLATION; ANIMALS; ASTHMA; DIET; DIETARY FIBER; DISEASE MODELS, ANIMAL; EPIGENESIS, GENETIC; FATTY ACIDS, VOLATILE; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GASTROINTESTINAL MICROBIOME; HISTONE DEACETYLASES; MICE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; T-LYMPHOCYTES, REGULATORY;

EID: 84934987107     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8320     Document Type: Article

References (68)

1. Strachan, D. P. Family size, infection and atopy: the first decade of the "hygiene hypothesis". Thorax 55(Suppl 1): S2-10 (2000).
2. Strachan, D. P. Hay fever, hygiene, and household size. BMJ 299, 1259-1260 (1989).
3. Maslowski, K. M., Mackay, C. R. Diet, gut microbiota and immune responses. Nat. Immunol. 12, 5-9 (2011).
4. Thorburn, A. N., Macia, L., Mackay, C. R. Diet, metabolites, and "Westernlifestyle" inflammatory diseases. Immunity 40, 833-842 (2014).
5. Devereux, G. The increase in the prevalence of asthma and allergy: food for thought. Nat. Rev. Immunol. 6, 869-874 (2006).
6. Trompette, A. et al. Gut microbiota metabolism of dietary fibre influences allergic airway disease and hematopoiesis. Nat.Med. 20, 159-166 (2014).
7. Noverr, M. C., Huffnagle, G. B. Does the microbiota regulate immune responses outside the gut? Trends Microbiol. 12, 562-568 (2004).
8. Dorrestein, P. C., Mazmanian, S. K., Knight, R. Finding the missing links among metabolites, microbes, and the host. Immunity 40, 824-832 (2014).
9. Kau, A. L., Ahern, P. P., Griffin, N. W., Goodman, A. L., Gordon, J. I. Human nutrition, the gut microbiome and the immune system. Nature 474, 327-336 (2011).
10. Boulet, L. P. Asthma and obesity. Clin. Exp. Allergy 43, 8-21 (2013).
11. Sin, D. D., Sutherland, E. R. Obesity and the lung: 4. Obesity and asthma. Thorax 63, 1018-1023 (2008).
12. Dixon, A. E. et al. An official American Thoracic Society Workshop report: obesity and asthma. Proc. Am. Thorac. Soc. 7, 325-335 (2010).
13. Jensen, M. E., Wood, L. G., Gibson, P. G. Obesity and childhood asthma-mechanisms and manifestations. Curr. Opin. Allergy Clin. Immunol. 12, 186-192 (2012).
14. Wood, L. G., Garg, M. L., Gibson, P. G. A high-fat challenge increases airway inflammation and impairs bronchodilator recovery in asthma. J. Allergy Clin. Immunol. 127, 1133-1140 (2011).
15. Wood, L. G. et al. Manipulating antioxidant intake in asthma: a randomized controlled trial. Am. J. Clin. Nutr. 96, 534-543 (2012).
16. Ellwood, P. et al. Do fast foods cause asthma, rhinoconjunctivitis and eczema? Global findings from the International Study of Asthma and Allergies in Childhood (ISAAC) phase three. Thorax 68, 351-360 (2013).
17. Wickens, K. et al. Fast foods-are they a risk factor for asthma? Allergy 60, 1537-1541 (2005).
18. Carey, O. J., Cookson, J. B., Britton, J., Tattersfield, A. E. The effect of lifestyle on wheeze, atopy, and bronchial hyperreactivity in Asian and white children. Am. J. Respir. Crit. Care Med. 154, 537-540 (1996).
19. Nagel, G., Weinmayr, G., Kleiner, A., Garcia-Marcos, L., Strachan, D. P. Effect of diet on asthma and allergic sensitisation in the International Study on Allergies and Asthma in Childhood (ISAAC) Phase Two. Thorax 65, 516-522 (2010).
20. Berthon, B. S., Macdonald-Wicks, L. K., Gibson, P. G., Wood, L. G. Investigation of the association between dietary intake, disease severity and airway inflammation in asthma. Respirology 18, 447-454 (2013).
21. Lloyd, C. M., Hawrylowicz, C. M. Regulatory T cells in asthma. Immunity 31, 438-449 (2009).
22. Holgate, S. T. The sentinel role of the airway epithelium in asthma pathogenesis. Immunol. Rev. 242, 205-219 (2011).
23. Thorburn, A. N. et al. Pneumococcal conjugate vaccine-induced regulatory T cells suppress the development of allergic airways disease. Thorax 65, 1053-1060 (2010).
24. Maslowski, K. M. et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461, 1282-1286 (2009).
25. Smith, P. M. et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341, 569-573 (2013).
26. Arpaia, N. et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504, 451-455 (2013).
27. Furusawa, Y. et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504, 446-450 (2013).
28. Faith, J. J., Ahern, P. P., Ridaura, V. K., Cheng, J., Gordon, J. I. Identifying gut microbe-host phenotype relationships using combinatorial communities in gnotobiotic mice. Sci. Transl. Med. 6, 220ra211 (2014).
29. Fukuda, S. et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469, 543-547 (2011).
30. Macia, L. et al. Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat. Commun. 6, 6734 (2015).
31. Tao, R. et al. Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat. Med. 13, 1299-1307 (2007).
32. Marson, A. et al. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 445, 931-935 (2007).
33. Chen, G. Y. et al. Cutting edge: Broad expression of the FoxP3 locus in epithelial cells: a caution against early interpretation of fatal inflammatory diseases following in vivo depletion of FoxP3-expressing cells. J.Immunol. 180, 5163-5166 (2008).
34. Conrad, M. L. et al. Maternal TLR signaling is required for prenatal asthma protection by the nonpathogenic microbe Acinetobacter lwoffii F78. J. Exp. Med. 206, 2869-2877 (2009).
35. Pomare, E. W., Branch, W. J., Cummings, J. H. Carbohydrate fermentation in the human colon and its relation to acetate concentrations in venous blood. J. Clin. Invest. 75, 1448-1454 (1985).
36. Morita, R., Ukyo, N., Furuya, M., Uchiyama, T., Hori, T. Atrial natriuretic peptide polarizes human dendritic cells toward a Th2-promoting phenotype through its receptor guanylyl cyclase-coupled receptor A. J. Immunol. 170, 5869-5875 (2003).
37. David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559-563 (2014).
38. De Filippo, C. et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl Acad. Sci. USA 107, 14691-14696 (2010).
39. Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222-227 (2012).
40. Del Campo, R. et al. Improvement of digestive health and reduction in proteobacterial populations in the gut microbiota of cystic fibrosis patients using a Lactobacillus reuteri probiotic preparation: A double blind prospective study. J. Cyst. Fibros. 13, 716-722 (2014).
41. De Cruz, P. et al. Specific mucosa-associated microbiota in Crohn's disease at the time of resection are associated with early disease recurrence: A Pilot Study. J. Gastroenterol. Hepatol. 30, 268-278 (2014).
42. Kearley, J., Barker, J. E., Robinson, D. S., Lloyd, C. M. Resolution of airway inflammation and hyperreactivity after in vivo transfer of CD4\+CD25\+ regulatory T cells is interleukin 10 dependent. J. Exp. Med. 202, 1539-1547 (2005).
43. Hou, X. X. et al. Characteristics of histone deacetylase 9 in peripheral blood of patients with bronchial asthma. Zhonghua Jie He He Hu Xi Za Zhi 35, 340-344 (2012).
44. Kwon, D. H. et al. Steep left ventricle to aortic root angle and hypertrophic obstructive cardiomyopathy: study of a novel association using threedimensional multimodality imaging. Heart 95, 1784-1791 (2009).
45. Karmodiya, K., Krebs, A. R., Oulad-Abdelghani, M., Kimura, H., Tora, L. H3K9 and H3K14 acetylation co-occur at many gene regulatory elements, while H3K14ac marks a subset of inactive inducible promoters in mouse embryonic stem cells. BMC Genomics 13, 424 (2012).
46. Gluckman, P. D., Hanson, M. A., Cooper, C., Thornburg, K. L. Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med. 359, 61-73 (2008).
47. Jackson, D. J. et al. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am. J. Respir. Crit. Care Med. 178, 667-672 (2008).
48. Dodge, R., Martinez, F. D., Cline, M. G., Lebowitz, M. D., Burrows, B. Early childhood respiratory symptoms and the subsequent diagnosis of asthma. J. Allergy Clin. Immunol. 98, 48-54 (1996).
49. Lima, J. J. et al. A polymorphism in the NPPA gene associates with asthma. Clin. Exp. Allergy 38, 1117-1123 (2008).
50. Rogers, A. J. et al. Assessing the reproducibility of asthma candidate gene associations, using genome-wide data. Am. J. Respir. Crit. Care Med. 179, 1084-1090 (2009).
51. Kandasamy, R. et al. Isatin down-regulates expression of atrial natriuretic peptide receptor A and inhibits airway inflammation in a mouse model of allergic asthma. Int. Immunopharmacol. 10, 218-225 (2010).
52. Mohapatra, S. S., Lockey, R. F., Vesely, D. L., Gower, Jr. W. R. Natriuretic peptides and genesis of asthma: an emerging paradigm? J. Allergy Clin. Immunol. 114, 520-526 (2004).
53. Baine, I., Basu, S., Ames, R., Sellers, R. S., Macian, F. Helios induces epigenetic silencing of IL2 gene expression in regulatory T cells. J. Immunol. 190, 1008-1016 (2013).
54. Reik, W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425-432 (2007).
55. Eder, W., Ege, M. J., von Mutius, E. The asthma epidemic. N. Engl. J. Med. 355, 2226-2235 (2006).
56. Barker, D. J. et al. Fetal nutrition and cardiovascular disease in adult life. Lancet 341, 938-941 (1993).
57. Sheedy, J. R., Ebeling, P. R., Gooley, P. R., McConville, M. J. A sample preparation protocol for 1H nuclear magnetic resonance studies of watersoluble metabolites in blood and urine. Anal. Biochem. 398, 263-265 (2010).
58. Yu, Z., Morrison, M. Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques 36, 808-812 (2004).
59. Quinlan, A. R., Stewart, D. A., Stromberg, M. P., Marth, G. T. Pyrobayes: an improved base caller for SNP discovery in pyrosequences. Nat. Methods 5, 179-181 (2008).
60. Ashelford, K. E., Chuzhanova, N. A., Fry, J. C., Jones, A. J., Weightman, A. J. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl. Environ. Microbiol. 71, 7724-7736 (2005).
61. Bragg, L., Stone, G., Imelfort, M., Hugenholtz, P., Tyson, G. W. Fast, accurate error-correction of amplicon pyrosequences using Acacia. Nat. Methods 9, 425-426 (2012).
62. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336 (2010).
63. Thorburn, A. N., Foster, P. S., Gibson, P. G., Hansbro, P. M. Components of Streptococcus pneumoniae suppress allergic airways disease and NKT cells by inducing regulatory T cells. J. Immunol. 188, 4611-4620 (2012).
64. Thorburn, A. N. et al. Pneumococcal components induce regulatory T cells that attenuate the development of allergic airways disease by deviating and suppressing the immune response to allergen. J. Immunol. 191, 4112-4120 (2013).
65. Murphy, V. E., Powell, H., Wark, P. A. B., Gibson, P. G. A prospective study of respiratory viral infection in pregnant women with and without asthma. CHEST J. 144, 420-427 (2013).
66. Mattes, J., Murphy, V. E., Powell, H., Gibson, P. G. Prenatal origins of bronchiolitis: protective effect of optimised asthma management during pregnancy. Thorax 69, 383-384 (2013).
67. Powell, C. V. E., McNamara, P., Solis, A., Shaw, N. J. A parent completed questionnaire to describe the patterns of wheezing and other respiratory symptoms in infants and preschool children. Arch.Dis.Childhood 87, 376-379 (2002).
68. McLernon, P. C., Wood, L. G., Murphy, V. E., Hodyl, N. A., Clifton, V. L. Circulating antioxidant profile of pregnant women with asthma. Clin. Nutr. 31, 99-107 (2012).